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Ovule and Seed Development in Droseraceae

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Ovule and Seed Development in Droseraceae Acta Bot. Need. 38(3), September 1989, p. 295-311 Ovule and seed development in Droseraceae F.D. Boesewinkel Hugo de Vries Laboratorium, University of Amsterdam, Kruislaan 318,1098 SM Amsterdam SUMMARY A structural analysis ofovule and seed development in the fourgenera of the Droseraceae is given. The ovule primordia ofthe Droseraceaeare dizonate. The dermalin The ovules of integuments are origin. Dionaea, Aldrovandaand Drosera are characterized by nucellarelongation and strongly enlarged cells of the nucellarepidermis. This featureis lacking in Drosophyllum. The differences in the seed coat ofthe four generaare mainly due to variationsin the differentiationof the testa. Drosophyllum has an endotestalcrystal layer, Dionaeaand Aldrovandaare exotestal andexo-/endotestal respectively, whereas Drosera has a less complex testa. Contrary to the testa, the tegmenshows more correspondence. It consists of an endotegmic sclerotized orpigment layer and crushed in of the variable remaining outer tegmic layers. As a consequence, spite basic similar testa structure the seed coat structure is in the four genera. In Drosophyllum, Dionaeaand Drosera the sclerotic layers ofthe seed coat are not lignified. Although the seed dimensionsare different, the operculate seeds with starchy endosperm and smallembryo have a similar construction. From the point ofview of the seed anatomy, the four genera are correctly placed in the Droseraceae. Key-words: Droseraceae, endotegmen, operculum, seed anatomy. INTRODUCTION The family Droseraceae consists of carnivorous herbs and comprises the monotypic and Aldrovanda and the with three genera Drosophyllum, Dionaea larger genusDrosera subgenera and about 85 species. Drosophyllum, Dionaeaand Aldrovandaare sharply delimitedgenera, the first two also with a narrow geographical distribution (Diels 1936; Takahashi & Sohma 1982). Droso- isendemic the of the Mediterranean the phyllum to western part region, Dionaea, Venusfly- the South-east whereas Aldrovanda trap, is endemic to of the USA, has a disjunct area, extending from Europe through Central Africa, Indiaand Japan to Australia.The genus Drosera is cosmopolitan with the greatest speciation in Australiaand New Zealand. The suffruticose Drosophyllum grows on sandy soils under pine trees. The other and other but is herbaceous genera occur in bogs on waterlogged soils, Aldrovanda a These show their submerged water-plant (Heywood 1978). genera adaptations to water- rich environment. The most typical character of the Droseraceae is theircarnivory. For this the have different and anatomical purpose genera morphological adaptations. Drosophyllum and Drosera resemble each other in their external morphology and trap 295 296 F. D. BOESEWINKEL Their consists of of stalked mechanism (fly-paper type). trap a great number glands, mainly on the leaves, which exude sticky droplets with digestive enzymes. Contrary to Drosophyllum, in Drosera the tentacles, and to a certain degree also the leaves, have the ability to envelop the captured prey by performing slow incurving movements. Dionaea and Aldrovanda have two-lobed leafblades which close immediately when an animal gives an appropriate stimulus to the trigger hairs on the leafsurface (active trap). It is assumed that small animals the Droseraceae theirlow by digesting may supplement nitrogen or phosphorous supply in their nutritionally poor environments. The is one-loculed and consists of four three fused syncarpous ovary five, or carpels with their margins. All genera have numerous seeds per fruit, but Drosera often has a large amount ofdust seeds. The fruit is a loculicidalcapsule which does not open in Aldrovanda. The is basal and the ovules and either placentation or parietal are anatropous, bitegmic crassinucellate or tenuinucellate in some Drosera species, with the micropyle formed by the inner integument (Pace 1912; Netolitzky 1926; Davis 1966; Corner 1976; Favard 1963). Smith (1929) and Teryokhin (1986) studied the embryology and seed coat anatomy of and Aldrovanda. The chalazal into of Dionaea megaspore develops a Polygonum type Patankar embryo sac (Davis 1966; 1956). The lateral nucellar cells become radially elongated to form a conspicuous jacket around the embryo sac. The endosperm formation is initially nuclearand the chalazal part has a haustorialfunction. According to Cronquist (1981) the fleshy and solid endosperm is granular and starchy as well as oily and proteinaceous. The small embryo is situated below the micropyle and at germination the root pushes a small operculum, formed by the tips of the innerintegument, outwards (Netolitzky 1926; Corner 1976). The tips of the cotyledons have a haustorial characterand in Drosophyllum and Aldrovandathe cotyledons remainenclosed within the seed during germination (Diels 1906). The dataon the seed coat structure are scattered in literature.Corners’ (1976) review on is the family mainly basedon Netolitzky (1926) and gives a misinterpretation of the tegmic layers and nucellar remnants in Drosophyllum. Corner’s suggestion of a pachychalazal seed in is also not correct. The in the of Dionaea genera agree presence an endotegmic, tanniniferouslayer and crushed outer tegmic layers. Drosophyllum has an endotestal crystal layer and a partly sclerotized tegmen (Netolitzky 1926); the seed coat of Dionaea is exotestal (Smith 1929); Aldrovanda combines an exo- and endotesta (Teryokhin 1986) and Drosera has a less complex testa. Several authors have questioned the placement of Drosophyllum, Dionaea and Aldrovanda in Droseraceae and proposed the separate families Dionaeaceae Dum. and Aldrovandaceae Nak. (See Takakashi & Sohma 1982). In most recent classifications the four in genera are placed together Droseraceae. The opinions concerning the superfamilial relationships of the Droseraceae are rather conflicting. The Droseraceae have often been connected with the insectivorous families Sarraceniaceae and Nepenthaceae and classified in Sarraceniales or Nepenthales (Hutchinson 1973; Melchior 1964; Takhtajan 1973; Cronquist 1981).Other familiesoften suggested as close relatives are Saxifragaceae, Crassulaceae and Parnassiaceae. During the last 120 years there are two opposed opinions as regards the superordinal classificationof the family. According to Cronquist (1981) the Droseraceae belong to the Dillenialeanalliance. Dahlgren (1980) was initially of the same opinion, but in his revised system (Dahlgren 1983) he agrees with Takhtajan (1973), Heywood (1978) and Thorne (1983)and transferred the family to the Rosaleanalliance. OVULE AND SEED DEVELOPMENT IN DROSERACEAE 297 The aim of this study was to enlarge the knowledge of the structure of ovules and seeds of Droseraceae, to draw conclusions concerning the mutual relationships of the genera and to assess the familieswith which the Droseraceae are related. MATERIALS AND METHODS Developing flowers and fruits of Drosophyllum lusitanicum L. Link, Dionaea muscipula Ellis, Drosera capensis L. and D. intermediaHayne were collectedin the Hortus Botanicus, University of Amsterdam. Also studied were seeds of D. capillaris Poir, D. natalensis Diels, D. rotundifolia L., D. regia Stephens and D. spathulata Labill and other species (14 in total). Craf The plant materialwas fixed in F.A. A. or mixtures (Sass 1958). Sections were made by the standard microtome technique afterembedding in paraffin wax (dehydration in an ethanol/tertiary butyl alcohol series) or in glycol methacrylate (dehydration inan ethanol/ n-butyl alcohol series). In the latter case the sections were stained with the periodic acidic Schiff’s reaction and counterstainedwith aqueous toluidine blue (Sidman et al. 1961). Phloroglucinol-HCl, Sudan IV, ruthenium red, IKI, and nigrosine solutions wereused for the identification of lignins, fats, pectins, starch and proteins, respectively. In order to remove epicuticular wax structures Drosera seeds were immersedfor 2 h in chloroform. For scanning electron microscopy (SEM) untreated or critical point-dried specimens were gold- or gold/palladium-sputtercoated for about 2-5 min and studied on a Cambridge stereoscan mark Ha or an ISI DS 130. RESULTS Drosophyllum lusitanicum Ovule development ofD. lusitanicum. The ovule primordium is dizonate and consists of the descendants ofthe original dermal(1,) and subdermal layer (1 ) ofthe placenta (Fig. la 2 & b). The dermal layer only divides anticlinally and surrounds the subdermal tissue. Shortly before the initiationof the innerintegument (ii) the subdermal archespore differ- entiates (Fig. 1c) and later cuts off 1-2 layers of parietal cells situated as usual above the archespore (Fig. Id-f). The tetrad is linearand the chalazal megaspore develops into the embryo sac (Fig. Ig). The nucellusbecomes massive mainly by periclinal divisionsaround the embryo sac (es). The innerintegument (ii) is initiateddermally as a complete ring-wall two cells broad (Fig. Ic-e) somewhat earlier than, or simultaneously with, the outer integument (oi). The oi is also initiatedas a dermal wall two-three cells broad, but the wall side is there dermal is absent at the raphal or only represented by a small cap in the mature ovule. The ii is at first two-three layered, but it becomes four-layered, mainly by periclinal divisions of its inner layer, when it has overgrown the nucellus. The oi is initially about three-layered (Fig. le-g) and remains so until the ovule is mature. Especially in its earlier stages the oi remains much shorter than the ii. The mature ovule ofD. lusitanicum. The ovule is anatropous, bitegmic and crassinucellate.
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